Retinotectal Projection Pattern Research Articles

Rostrocaudal polarity formation of chick optic tectum.

The optic tectum receives retinal fibers in a topographically ordered manner. For the formation of the precise connections, the tectum is believed to be positionally specified by gradients of molecules along axes. Rostrocaudal polarity of the tectum is first detectable at embryonic day 2 (E2) in the chick, by the caudorostral gradient of en expression, then by the rostrocaudal gradient of cytoarchitectonic development. Tectum rotation experiments showed that tectum rostrocaudal polarity is not determined at around 10-somite stage, but is fixed on E3. Ectopic tectum was produced in the diencephalon by transplanting the mesencephalic alar plate heterotopically. In the ectopic tectum, en expression was weakest at the caudal (nearest to the host diencephalo-mesencephalon junction) and strongest at the rostral end. Consequently, the pattern of en expression in the host and ectopic tecta was nearly a mirror image. Retinal fibers projected to the ectopic tectum in a topographic order in accordance with the inverted gradient of the en expression pattern. Ectopic tecta was also produced by heterochronal transplantations between E3 host and E2 donor, where the en pattern was preserved. Retinotectal projection pattern was also preserved, suggesting that en expression patterns are followed by retinotopic order with regard to rostrocaudal polarity.

Rostrocaudal polarity of the tectum in birds: Correlation of en gradient and topographic order in retinotectal projection

Rostrocaudal polarity of the tectum is first detectable at embryonic day 2 (E2) in the chick by the rostrocaudal gradient of en expression. When ectopic tectum is produced by heterotopic transplantation at E2 in the diencephalon, the gradient of en expression is inverted from the host polarity by environmental influences. Here we report that the retinal fibers project to the ectopic tectum in a topographic order in accord with the inverted gradient of en expression. Moreover, if ectopic tectum was produced at E3, when the en pattern was preserved, the retinotectal projection pattern was also in accord with the en pattern, suggesting that rostrocaudal polarity of retinotectal order follows en expression patterns.

Establishment of rostrocaudal polarity in tectal primordium: engrailed expression and subsequent tectal polarity

In the E4 (embryonic day 4) chick tectal primordium, engrailed expression is strong at the caudal end and gradually weakens toward the rostral end. We used quail-chick chimeric tecta to investigate how the caudorostral gradient of engrailed expression is established and whether it is correlated with the subsequent rostrocaudal polarity of tectal development. To examine the positional value of the tectal primordium, we produced ectopic tecta in the diencephalon by transplanting a part of the mesencephalic alar plate heterotopically. In the ectopic tectum, the gradient of the engrailed expression reversed and the strength of the expression was dependent on the distance from the mes-diencephalon junction; the nearer the ectopic tectum was to the junction, the weaker the expression was. Consequently, the pattern of the engrailed expression in the host and ectopic tecta was nearly a mirror image, suggesting the existence of a repressive influence around the mes-diencephalon junction on the engrailed expression. We examined cytoarchitectonic development in the ectopic tecta, which normally proceeds in a gradient along the rostrocaudal axis; the rostral shows more advanced lamination than the caudal. In contrast, the caudal part of the ectopic tecta (near to the mes-diencephalon junction) showed more advanced lamination than the rostral. In both the host and ectopic tecta, advanced lamination was observed where the engrailed expression was repressed, and vice versa. Next we studied the correlation between engrailed expression and retinotectal projection from a view of plasticity and rigidity of rostrocaudal polarity in the tectum. We produced ectopic tecta by anisochronal transplantations between E3 host and E2 donor, and showed that there is little repressive influence at E3 around the mes-diencephalon junction. We then made chimeric double-rostral tectum (caudal half of it was replaced by rostral half of the donor tectum) or double-caudal tectum at E3. The transplants kept their original staining pattern in hosts. Consequently, the chimeric tecta showed wholly negative or positive staining of engrailed protein on the grafted side. In such tecta retinotectal projection pattern was disturbed as if the transplants retained their original position-specific characters. We propose from these heterotopic and anisochronal experiments that the engrailed expression can be a marker for subsequent rostrocaudal polarity in the tectum, both as regards cytoarchitectonic development and retinotectal projection.

Adaptations for spatial vision in sharks

The revelation that sharks as a group are not simply all-rod, nocturnal vertebrates has called for a new perspective on their spatial visual capabilities. Using the lemon shark (Negaprion brevirostris) as a model species, selected components of spatial vision in sharks have been investigated. The physiological optics of the eye have been modeled with a schematic eye for the lemon shark, the first such model for an elasmobranch species. Retinal cone and ganglion cell topography and retinotectal projection pattern have been mapped completely for the first time in an elasmobranch. These topographic maps reveal a prominent visual streak, a functional specialization that is correlated with the lemon shark's visual behavior and habitat. Evidence in the literature of similar specializations for spatial vision in other elasmobranchs signifies that the lemon shark is not a special case. Assessments of the quality of shark vision should consider the sensory niches of these animals in their specific marine environments, as well as the phylogenetic and ontogenetic diversity within the group.

Aspects of retinotectal topography: Tectal magnification of specialized retinal areas and a possible center for binocular input

Retinotectal projection patterns range from approximately linear representations of visual field coordinates onto the midbrain roof to non-linear projections of visual space with areal magnifications. “Visual streaks” are magnified horizontal bands and reflect specializations of retinal fine structure, especially ganglion cell densities. Horizontal visual streaks are common in several vertebrate classes, including elasmobranchs and mammals. “Convexiclivate” foveae and their greatly expanded projections on the midbrain surface have been found in teleosts, reptiles, and birds. The nucleus corticalis of the teleostean midbrain contains neurons that can be activated by photic stimulation of both eyes, suggesting involvement in binocular vision.

Gradual appearance of a regulated retinotectal projection pattern in Xenopus laevis

The topographic projection pattern formed by the retinal ganglion cell axons in the tectum of the lower vertebrate appears to require positional cues that guide the optic nerve fibers to their appropriate targets. One approach to understanding these positional cues or “positional information” has been to investigate changes in the pattern of the retinotectal projection after surgical manipulation of the embryonic eyebud. Analysis of these apparent changes in the patterns of positional information in the eye, termed “pattern regulation,” may provide clues to both the nature of positional information and the mechanisms by which it is assigned to cells in the eyebud. Here we examine pattern regulation in the Xenopus visual system following the replacement of the temporal half of a right eyebud with the temporal half of a left eyebud. This manipulation requires that the left half-eyebud be inverted along its dorsoventral axis. Electrophysiological maps of these compound eyes in postmetamorphic frogs reveal regulated maps; the cells in the temporal half of the N rT l eye project to the tectum with a dorsoventral polarity appropriate for their position in the host eye and not appropriate for the original positions of the grafted cells in the donor eyebud. Paradoxically, the regulated patterns are not apparent in the projections of the original grafted eyebud cells during early larval development. Using fiber-tracing and electrophysiological mapping techniques, we now show that the regulated patterns appear gradually in the projections made by peripheral retinal cells added during mid-larval development. Because the regulation occurs relatively late in development and probably only in the peripheral retinal cells, simple models of epimorphic or morphallactic regulation do not appear to fit this system. Thus, new or more complex models must be invoked to explain the phenomenon of pattern regulation in the developing visual system of Xenopus.

Comparative neurology of the optic tectum in ray-finned fishes: patterns of lamination formed by retinotectal projections

Retinotectal projections were studied in 33 different species of Actinopterygii, the ray-finned fishes, with horseradish peroxidase and cobalt tracing techniques. The distribution of retinorecipient layers in the contralateral optic tectum was analyzed. In addition, the degree of differentiation of the stratum periventriculate, and the presence of ipsilateral retinotectal projections was examined. Retinofugal fibers are labeled in the stratum opticum (SO), stratum fibrosum et griseum superficiale (SFGS), stratum griseum centrale (SGC), stratum album centrale (SAC) and stratum periventriculare (SPV). Some species lack the projection to the SO, others lack the projection to the SGC, and a third group of fishes lack both projections. Five different patterns of retinorecipient tectal strata are distinguished. These patterns correlate with the species' taxonomic position. Evolutionary trends of tectal lamination and retinotectal innervation are described. The retinotectal projection patterns provide a useful indicator of phylogenetic relationships. Some of our data suggest different relationships between actinopterygian species than hitherto believed.

Alteration of the retinotectal map in Xenopus by antibodies to neural cell adhesion molecules.

The neural cell adhesion molecule (N-CAM) mediates neuron-neuron adhesion, is ubiquitous in the nervous system of developing and mature vertebrates, and undergoes major alterations in both amount and distribution during development. Perturbation of homophilic (N-CAM to N-CAM) binding by univalent fragments of specific anti-N-CAM antibodies has previously been found to alter neural tissue patterns in vitro. To show that significant alterations can also occur in vivo, antibodies to Xenopus N-CAM were embedded in agarose microcylinders and implanted in the tecta of juvenile Xenopus laevis frogs that were undergoing regeneration of their retinotectal projections; 1 week later, the effects of implantation on the projection pattern from the optic nerve were determined. Both polyclonal and monoclonal antibodies to N-CAM distorted the retinotectal projection pattern and greatly decreased the precision of the projection; these alterations recovered to near normal after an additional 3 weeks. Similar but smaller effects were obtained when normally developing froglets received tectal implants. In control animals, implants of immunoglobulins from preimmune serum and monoclonal antibodies not directed against N-CAM had little or no effect on the pattern. The results suggest that neuronal adhesion mediated by N-CAM is important in establishing and maintaining the precision and topography of neural patterns.

Axonal pathfinding in the absence of normal pathways and impulse activity

Retinal axons were challenged to grow to their targets both along abnormal pathways and in the absence of impulse activity. Eye primordia were first transplanted from normal to ectopic sites in axolotl embryos. Most of the hosts were genetically eyeless, others were enucleated normal embryos. These axolotl embryos were then parabiotically joined to California newt embryos. Both operations were completed by stage 28, which is before axons have left the eye. The result of the parabiosis was a paralysis of the "eyeless" axolotl twin due to the newt's tetrodotoxin (TTX), while the newt twin remained normally active. When the axolotl twin reached early larval stage, about 1 week later, the projection from the silent transplanted retina was assessed using horseradish peroxidase (HRP) injections into the retina, after which the animals were killed and prepared histologically to reveal the presence of HRP in neuronal processes. The results from 17 such cases show normal topographic retinotectal projections: the dorsal retina projecting to the ventrolateral tectum, and the ventral retina projecting to the dorsomedial tectum. Unusual pathways were often taken to achieve these destinations. Control animals, both normal axolotl larvae developing alone and normal axolotl larvae parabiosed to newts, also showed the normal retinotectal projection patterns. These results indicate that the retinal projections in the experimental group were basically normal. Thus, fibers need neither impulse activity nor a particular pathway to navigate to their correct targets during development. Both factors can be eliminated simultaneously, yet retinal axons still find their way to the tectum and make an ordered map. This indicates that other factors, such as the chemoaffinity mechanisms proposed by Sperry (Sperry, R.W. (1963) Proc. Natl. Acad. Sci. U.S.A. 50: 703-710), may play a more major role in axonal pathfinding in this system.

An electrophysiological study of early retinotectal projection patterns during regeneration following optic nerve crush inside the cranium in Hyla moorei

The sequence of regeneration following intracranial optic nerve crush has been studied using electrophysological visual mapping in the frog Hyla moorei. Compared to our earlier series 9 with extracranial crush, the time course was slower and the intermediate projections more disorganized. It is suggested that the apparent discrepancy between the early patterns of regeneration in Xenopus 4 and Rana 5,6 compared to Hyla 9, fish 8 and newt 2, is not due to species differences but to the location of the lesion site.

An electrophysiological study of early retinotectal projection patterns during optic nerve regeneration in Hyla moorei

The sequence of regeneration of the optic nerve into the tectum has been studied using electrophysiological visual mapping in the frog, Hyla moorei. Some individuals were remapped to confirm the sequential nature of the changes described. The projection was retinotopic throughout regeneration. Multiunit receptive field sizes were initially large but progressively decreased to normal over approximately 30 days. The differences between these results and earlier studies are discussed.

Topographic projections of the retina and optic tectum upon the ventral lateral geniculate nucleus in the chick

The topographic projections of the retina upon the optic tectum and ventral lateral geniculate nucleus (GLv) of the chick were investigated by making small intraretinal injections of 3H-proline. The retinotectal projection pattern was similar to that described for the pigeon. The retinal projection to the GLv was also topographic and was restricted to the outermost lamina of the nucleus. The anteroposterior retinal axis was reversed in the GLv relative to its orientation in the tectum but the superoinferior axis was oriented identically in both. Furthermore, the posterior retina had an enlarged area of projection in the GLv similar to the enlarged area of retinotectal projection for the "red field" found in pigeons. The tectogeniculate projection was topographic and was confined to the outermost geniculate lamina. The second-order retinotopic map made by the tectogeniculate projections was in register with the retinogeniculate projection. Although the retinal and tectal projection areas were coextensive in the outermost geniculate lamina, the grain density distributions peaked at different points along a radial path through the geniculate laminae. Injections of HRP into the optic tectum led to very light retrograde labeling of a small population of GLv cells topographically corresponding to the tectogeniculate projection zone of the injection site. The data suggest that the chick GLv is comparable to the GLv of other non-primate mammals.

Pattern of retinotectal connections after retinal regeneration.

Pattern of retinotectal connections after retinal regeneration.J Cronly-DillonJ Cronly-DillonPublished Online:01 May 1968https://doi.org/10.1152/jn.1968.31.3.410MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformationCited ByMolecules, maps and gradients in the retinotectal projectionTrends in Neurosciences, Vol. 14, No. 12An electrophysiological study of early retinotectal projection patterns during regeneration following optic nerve crush inside the cranium in Hyla mooreiBrain Research, Vol. 269, No. 1An electrophysiological study of early retinotectal projection patterns during optic nerve regeneration inHyla mooreiBrain Research, Vol. 239, No. 2Retinotopic analysis of fiber pathways in the regenerating retinotectal system of the adult newt cynops pyrrhogasterBrain Research, Vol. 206, No. 1Involvement of retinal pigment epithelium in the genesis of locus specificities during retinal regeneration in the newtBrain Research, Vol. 162, No. 1Ganglion cell responses of the mudpuppy retina to flashing and moving stimuliVision Research, Vol. 16, No. 12An autoradiographic study of changes in the frog tectum after cutting the optic nerveBrain Research, Vol. 76, No. 2Specification of regenerating retinal ganglion cells in the adult newt,triturus cristatusBrain Research, Vol. 68, No. 2Anomalous retinal projection after removal of contralateral optic tectum in adult goldfishExperimental Neurology, Vol. 41, No. 3Tests for neuroplasticity in the anuran retinotectal systemExperimental Neurology, Vol. 40, No. 2Further studies on the restoration of the contralateral retinotectal projection following regeneration of the optic nerve in the frogBrain Research, Vol. 21, No. 2The depth distribution of visual units in the contralateral optic tectum following regeneration of the optic nerve in the frogBrain Research, Vol. 21, No. 2 More from this issue > Volume 31Issue 3May 1968Pages 410-8 https://doi.org/10.1152/jn.1968.31.3.410PubMed5687762History Published online 1 May 1968 Published in print 1 May 1968 Metrics